P2Y2 receptor activation opens pannexin-1 channels in rat carotid body type II cells: Potential role in amplifying the neurotransmitter ATP

Journal of Physiology

Volumn 590, Issue 17, 2012, Pages 4335-4350

  Zhang, Min ^a   Piskuric, Nikol A ^a   Vollmer, Cathy ^a   Nurse, Colin A ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM; GAP JUNCTION PROTEIN; MESSENGER RNA; PANNEXIN 1; PURINERGIC P2Y2 RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CAROTID BODY; CELL ACTIVATION; CELL FUNCTION; CELL TYPE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GENE EXPRESSION; GLIA CELL; IMMUNOLOCALIZATION; NERVE ENDING; NEUROTRANSMITTER RELEASE; NONHUMAN; NUCLEOTIDE SEQUENCE; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; RECEPTOR UPREGULATION; SENSORY NERVE CELL; SIGNAL TRANSDUCTION;

ADENOSINE TRIPHOSPHATE; ANIMALS; CALCIUM; CAROTID BODY; CELLS, CULTURED; CONNEXINS; ELECTROPHYSIOLOGICAL PHENOMENA; GENE EXPRESSION; MEMBRANE POTENTIALS; MODELS, NEUROLOGICAL; NERVE TISSUE PROTEINS; NEUROTRANSMITTER AGENTS; PARACRINE COMMUNICATION; RATS; RECEPTORS, PURINERGIC P2Y2; RNA, MESSENGER; SYNAPTIC TRANSMISSION;

EID: 84865592969     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2012.236265     Document Type: Article

References (42)

1. Bao L, Locovei S & Dahl G (2004). Pannexin membrane channels are mechanosensitive conduits for ATP. FEBS Lett 572, 65-68.
2. Barbe MT, Monyer H & Bruzzone R (2006). Cell-cell communication beyond connexins: the pannexin channels. Physiology (Bethesda) 21, 103-114.
3. Bruzzone R, Barbe MT, Jakob NJ & Monyer H (2005). Pharmacological properties of homomeric and heteromeric pannexin hemichannels expressed in Xenopus oocytes. J Neurochem 92, 1033-1043.
4. Campanucci VA, Dookhoo L, Vollmer C & Nurse CA (2012). Modulation of the carotid body sensory discharge by NO: An up-dated hypothesis. Respir Physiol Neurobiol (in press).
5. 2-chemoreceptors: role in nitric oxide-mediated efferent inhibition. J Neurosci 26, 9482-9493.
6. Conde SV & Monteiro EC (2004). Hypoxia induces adenosine release from the rat carotid body. J Neurochem 89, 1148-1156.
7. Conde SV, Monteiro EC, Rigual R, Obeso A & Gonzalez C (2012). Hypoxic intensity: a determinant for the contribution of ATP and adenosine to the genesis of carotid body chemosensory activity. J Appl Physiol 112, 2002-2010.
8. Drummond GB (2009). Reporting ethical matters in The Journal of Physiology: standards and advice. J Physiol 587, 713-719.
9. Dubyak GR (2009). Both sides now: multiple interactions of ATP with pannexin-1 hemichannels. Focus on "A permeant regulating its permeation pore: inhibition of pannexin 1 channels by ATP". Am J Physiol Cell Physiol 296, C235-241.
10. Duchen MR, Caddy KW, Kirby GC, Patterson DL, Ponte J & Biscoe TJ (1988). Biophysical studies of the cellular elements of the rabbit carotid body. Neuroscience 26, 291-311.
11. Eroglu C & Barres BA (2010). Regulation of synaptic connectivity by glia. Nature 468, 223-231.
12. Eyzaguirre C & Zapata P (1984). Perspectives in carotid body research. J Appl Physiol 57, 931-957.
13. Gonzalez C, Almaraz L, Obeso A & Rigual R (1994). Carotid body chemoreceptors: from natural stimuli to sensory discharges. Physiol Rev 74, 829-898.
14. Huang Y, Grinspan JB, Abrams CK & Scherer SS (2007a). Pannexin1 is expressed by neurons and glia but does not form functional gap junctions. Glia 55, 46-56.
15. Huang YJ, Maruyama Y, Dvoryanchikov G, Pereira E, Chaudhari N & Roper SD (2007b). The role of pannexin 1 hemichannels in ATP release and cell-cell communication in mouse taste buds. Proc Natl Acad Sci USA 104, 6436-6441.
16. Iglesias R, Dahl G, Qiu F, Spray DC & Scemes E (2009). Pannexin 1: the molecular substrate of astrocyte "hemichannels". J Neurosci 29, 7092-7097.
17. Iturriaga R & Alcayaga J (2004). Neurotransmission in the carotid body: transmitters and modulators between glomus cells and petrosal ganglion nerve terminals. Brain Res Brain Res Rev 47, 46-53.
18. Iturriaga R, Mokashi A & Lahiri S (1998). Anion exchanger and chloride channel in cat carotid body chemotransduction. J Auton Nerv Syst 70, 23-31.
19. Kondo H (2002). Are there gap junctions between chief (glomus, type I) cells in the carotid body chemoreceptor? A review. Microsc Res Tech 59, 227-233.
20. Lai CP, Bechberger JF, Thompson RJ, MacVicar BA, Bruzzone R & Naus CC (2007). Tumor-suppressive effects of pannexin 1 in C6 glioma cells. Cancer Res 67, 1545-1554.
21. Locovei S, Bao L & Dahl G (2006a). Pannexin 1 in erythrocytes: function without a gap. Proc Natl Acad Sci USA 103, 7655-7659.
22. Locovei S, Wang J & Dahl G (2006b). Activation of pannexin 1 channels by ATP through P2Y receptors and by cytoplasmic calcium. FEBS Lett 580, 239-244.
23. Ma W, Hui H, Pelegrin P & Surprenant A (2009). Pharmacological characterization of pannexin-1 currents expressed in mammalian cells. J Pharmacol Exp Ther 328, 409-418.
24. McDonald DM & Mitchell RA (1975). The innervation of glomus cells, ganglion cells and blood vessels in the rat carotid body: a quantitative ultrastructural analysis. J Neurocytol 4, 177-230.
25. MacVicar BA & Thompson RJ (2010). Non-junction functions of pannexin-1 channels. Trends Neurosci 33, 93-102.
26. Nurse CA (2005). Neurotransmission and neuromodulation in the chemosensory carotid body. Auton Neurosci 120, 1-9.
27. Nurse CA (2010). Neurotransmitter and neuromodulatory mechanisms at peripheral arterial chemoreceptors. Exp Physiol 95, 657-667.
28. Nurse CA & Fearon IM (2002). Carotid body chemoreceptors in dissociated cell culture. Microsc Res Tech 59, 249-255.
29. Pardal R, Ortega-Saenz P, Duran R & Lopez-Barneo J (2007). Glia-like stem cells sustain physiologic neurogenesis in the adult mammalian carotid body. Cell 131, 364-377.
30. Parpura V, Heneka MT, Montana V, Oliet SH, Schousboe A, Haydon PG, Stout RF Jr, Spray DC, Reichenbach A, Pannicke T, Pekny M, Pekna M, Zorec R & Verkhratsky A (2012). Glial cells in (patho)physiology. J Neurochem 121, 4-27.
31. i responses of rat aortic body type I cells and endogenous local neurons: comparison with carotid body cells. J Physiol 590, 2121-2135.
32. Prasad M, Fearon IM, Zhang M, Laing M, Vollmer C & Nurse CA (2001). Expression of P2X2 and P2X3 receptor subunits in rat carotid body afferent neurones: role in chemosensory signalling. J Physiol 537, 667-677.
33. Sridharan M, Adderley SP, Bowles EA, Egan TM, Stephenson AH, Ellsworth ML & Sprague RS (2010). Pannexin 1 is the conduit for low oxygen tension-induced ATP release from human erythrocytes. Am J Physiol Heart Circ Physiol 299, H1146-1152.
34. Thompson RJ & Macvicar BA (2008). Connexin and pannexin hemichannels of neurons and astrocytes. Channels (Austin) 2, 81-86.
35. von Kugelgen I (2006). Pharmacological profiles of cloned mammalian P2Y-receptor subtypes. Pharmacol Ther 110, 415-432.
36. 2+ release in type II cells of the rat carotid body. J Physiol 549, 739-747.
37. Xu J, Xu F, Tse FW & Tse A (2005). ATP inhibits the hypoxia response in type I cells of rat carotid bodies. J Neurochem 92, 1419-1430.
38. Yen MR & Saier MH Jr (2007). Gap junctional proteins of animals: the innexin/pannexin superfamily. Prog Biophys Mol Biol 94, 5-14.
39. Zapata P (2007). Is ATP a suitable co-transmitter in carotid body arterial chemoreceptors? Respir Physiol Neurobiol 157, 106-115.
40. 2/pH chemosensory signaling in co-cultures of rat carotid body receptors and petrosal neurons: role of ATP and ACh. J Neurophysiol 92, 3433-3445.
41. Zhang M, Zhong H, Vollmer C & Nurse CA (2000). Co-release of ATP and ACh mediates hypoxic signalling at rat carotid body chemoreceptors. J Physiol 525, 143-158.
42. Zhong H, Zhang M & Nurse CA (1997). Synapse formation and hypoxic signalling in co-cultures of rat petrosal neurones and carotid body type 1 cells. J Physiol 503, 599-612.